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PLoS Biology May 2020Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial... (Comparative Study)
Comparative Study
Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal surrounding, a behavior known as whisking. Here, we investigated the contingency of whisking kinematics on the animal's behavioral context that arises from both internal processes (attention and expectations) and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at high temporal resolution in 2 experimental contexts-freely moving or head-fixed-and 2 spatial sensory configurations-a single row or 3 caudal whiskers on each side of the snout. We found that rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness and imposed head fixation exposed a backward redistribution of sensorimotor exploratory resources. Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head- and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining resources. In sum, this work shows that rats adapt their active exploratory behavior in a homeostatic attempt to preserve sensorimotor coverage under changing environmental conditions and changing sensory capacities, including those imposed by various laboratory conditions.
Topics: Adaptation, Physiological; Animals; Biomechanical Phenomena; Exploratory Behavior; Feedback, Sensory; Head Movements; Locomotion; Male; Rats, Wistar; Vibrissae
PubMed: 32453721
DOI: 10.1371/journal.pbio.3000571 -
PLoS Biology Oct 2020The array of vibrissae on a rat's face is the first stage in a high-resolution tactile sensing system. Progressing from rostral to caudal in any vibrissae row results in...
The array of vibrissae on a rat's face is the first stage in a high-resolution tactile sensing system. Progressing from rostral to caudal in any vibrissae row results in an increase in whisker length and thickness. This may, in turn, provide a systematic map of separate tactile channels governed by the mechanical properties of the whiskers. To examine whether this map is expressed in a location-dependent transformation of tactile signals into whisker vibrations and neuronal responses, we monitored whiskers' movements across various surfaces and edges. We found a robust rostral-caudal (R-C) gradient of tactile information transmission in which rostral shorter vibrissae displayed a higher sensitivity and bigger differences in response to different textures, whereas longer caudal vibrissae were less sensitive. This gradient is evident in several dynamic properties of vibrissae trajectories. As rodents sample the environment with multiple vibrissae, we found that combining tactile signals from multiple vibrissae resulted in an increased sensitivity and bigger differences in response to the different textures. Nonetheless, we found that texture identity is not represented spatially across the whisker pad. Based on the responses of first-order sensory neurons, we found that they adhere to the tactile information conveyed by the vibrissae. That is, neurons innervating rostral vibrissae were better suited for texture discrimination, whereas neurons innervating caudal vibrissae were more suited for edge detection. These results suggest that the whisker array in rodents forms a sensory structure in which different facets of tactile information are transmitted through location-dependent gradient of vibrissae on the rat's face.
Topics: Animals; Biomechanical Phenomena; Male; Neurons; Rats, Sprague-Dawley; Touch Perception; Trigeminal Ganglion; Vibrissae
PubMed: 33090990
DOI: 10.1371/journal.pbio.3000699 -
Journal of Neurophysiology Jun 2004The vibrissa sensory system is a key model for investigating principles of sensory processing. Specific frequency ranges of vibrissa motion, generated by rodent sensory... (Review)
Review
The vibrissa sensory system is a key model for investigating principles of sensory processing. Specific frequency ranges of vibrissa motion, generated by rodent sensory behaviors (e.g., active exploration or resting) and by stimulus features, characterize perception by this system. During active exploration, rats typically sweep their vibrissae at approximately 4-12 Hz against and over tactual surfaces, and during rest or quiescence, their vibrissae are typically still (<1 Hz). When a vibrissa is swept over an object, microgeometric surface features (e.g., grains on sandpaper) likely create higher frequency vibrissa vibrations that are greater than or equal to several hundred Hertz. In this article, I first review thalamic and cortical neural responses to vibrissa stimulation at 1-40 Hz. I then propose that neural dynamics optimize the detection of stimuli in low-frequency contexts (e.g., 1 Hz) and the discrimination of stimuli in the whisking frequency range. In the third section, I describe how the intrinsic biomechanical properties of vibrissae, their ability to resonate when stimulated at specific frequencies, may promote detection and discrimination of high-frequency inputs, including textured surfaces. In the final section, I hypothesize that distinct low- and high-frequency processing modes may exist in the somatosensory cortex (SI), such that neural responses to stimuli at 1-40 Hz do not necessarily predict responses to higher frequency inputs. In total, these studies show that several frequency-specific mechanisms impact information transmission in the vibrissa sensory system and suggest that these properties play a crucial role in perception.
Topics: Action Potentials; Animals; Humans; Neurons, Afferent; Vibrissae
PubMed: 15136599
DOI: 10.1152/jn.00925.2003 -
The Journal of Neuroscience : the... Apr 2014Rodents use their whiskers to detect a variety of tactile features of their environment. They do so by using two functionally distinct whisker systems: the...
Rodents use their whiskers to detect a variety of tactile features of their environment. They do so by using two functionally distinct whisker systems: the macrovibrissae and microvibrissae. To determine the functional role of unexplored microvibrissae, we recorded from the cortical area representing the frontobuccal pad in anesthetized rats while presenting moving textures of varying coarseness. We find that surface coarseness is coded by the discharge rates of frontobuccal pad cortical neurons. Cortical neurons can use this response measure to robustly and reliably discriminate between the different textures. While neuronal discharge rates carry tactile information, the highly reproducible firing patterns of these neurons suggest that a single spike train may contain sufficient information to encode the stimulus. Together, these results indicate that rodents may use their microvibrissae to distinguish between surfaces having subtly different textures and shapes.
Topics: Action Potentials; Animals; Discrimination, Psychological; Male; Rats; Rats, Sprague-Dawley; Somatosensory Cortex; Touch; Touch Perception; Vibrissae
PubMed: 24719091
DOI: 10.1523/JNEUROSCI.4217-13.2014 -
Current Biology : CB May 2023Cortical activity patterns occupy a small subset of possible network states. If this is due to intrinsic network properties, microstimulation of sensory cortex should...
Cortical activity patterns occupy a small subset of possible network states. If this is due to intrinsic network properties, microstimulation of sensory cortex should evoke activity patterns resembling those observed during natural sensory input. Here, we use optical microstimulation of virally transfected layer 2/3 pyramidal neurons in the mouse primary vibrissal somatosensory cortex to compare artificially evoked activity with natural activity evoked by whisker touch and movement ("whisking"). We find that photostimulation engages touch- but not whisking-responsive neurons more than expected by chance. Neurons that respond to photostimulation and touch or to touch alone exhibit higher spontaneous pairwise correlations than purely photoresponsive neurons. Exposure to several days of simultaneous touch and optogenetic stimulation raises both overlap and spontaneous activity correlations among touch and photoresponsive neurons. We thus find that cortical microstimulation engages existing cortical representations and that repeated co-presentation of natural and artificial stimulation enhances this effect.
Topics: Mice; Animals; Somatosensory Cortex; Parietal Lobe; Movement; Touch; Touch Perception; Vibrissae
PubMed: 37130521
DOI: 10.1016/j.cub.2023.03.085 -
Scientific Reports Jun 2021Neuronal activities underlying a percept are constrained by the physics of sensory signals. In the tactile sense such constraints are frictional stick-slip events,...
Neuronal activities underlying a percept are constrained by the physics of sensory signals. In the tactile sense such constraints are frictional stick-slip events, occurring, amongst other vibrotactile features, when tactile sensors are in contact with objects. We reveal new biomechanical phenomena about the transmission of these microNewton forces at the tip of a rat's whisker, where they occur, to the base where they engage primary afferents. Using high resolution videography and accurate measurement of axial and normal forces at the follicle, we show that the conical and curved rat whisker acts as a sign-converting amplification filter for moment to robustly engage primary afferents. Furthermore, we present a model based on geometrically nonlinear Cosserat rod theory and a friction model that recreates the observed whole-beam whisker dynamics. The model quantifies the relation between kinematics (positions and velocities) and dynamic variables (forces and moments). Thus, only videographic assessment of acceleration is required to estimate forces and moments measured by the primary afferents. Our study highlights how sensory systems deal with complex physical constraints of perceptual targets and sensors.
Topics: Animals; Male; Rats; Rats, Sprague-Dawley; Touch; Touch Perception; Vibrissae
PubMed: 34193889
DOI: 10.1038/s41598-021-92770-3 -
Neuroscience Jan 2018The world view of rodents is largely determined by sensation on two length scales. One is within the animal's peri-personal space; sensorimotor control on this scale... (Review)
Review
The world view of rodents is largely determined by sensation on two length scales. One is within the animal's peri-personal space; sensorimotor control on this scale involves active movements of the nose, tongue, head, and vibrissa, along with sniffing to determine olfactory clues. The second scale involves the detection of more distant space through vision and audition; these detection processes also impact repositioning of the head, eyes, and ears. Here we focus on orofacial motor actions, primarily vibrissa-based touch but including nose twitching, head bobbing, and licking, that control sensation at short, peri-personal distances. The orofacial nuclei for control of the motor plants, as well as primary and secondary sensory nuclei associated with these motor actions, lie within the hindbrain. The current data support three themes: First, the position of the sensors is determined by the summation of two drive signals, i.e., a fast rhythmic component and an evolving orienting component. Second, the rhythmic component is coordinated across all orofacial motor actions and is phase-locked to sniffing as the animal explores. Reverse engineering reveals that the preBötzinger inspiratory complex provides the reset to the relevant premotor oscillators. Third, direct feedback from somatosensory trigeminal nuclei can rapidly alter motion of the sensors. This feedback is disynaptic and can be tuned by high-level inputs. A holistic model for the coordination of orofacial motor actions into behaviors will encompass feedback pathways through the midbrain and forebrain, as well as hindbrain areas.
Topics: Animals; Behavior, Animal; Brain Stem; Facial Nucleus; Motor Activity; Mouth; Neural Pathways; Rodentia; Sensation; Touch Perception; Vibrissae
PubMed: 28843993
DOI: 10.1016/j.neuroscience.2017.08.034 -
Current Opinion in Neurobiology Dec 2018In the rodent somatosensory system, the disproportionally large whisker representation and their specialization into barrel-shaped units in the different sensory relays... (Review)
Review
In the rodent somatosensory system, the disproportionally large whisker representation and their specialization into barrel-shaped units in the different sensory relays has offered experimentalists with an ideal tool to identify mechanisms involved in brain map formation. These combine three intertwined constraints: Firstly, fasciculation of the incoming axons; secondly, early neural activity; finally, molecular patterning. Sophisticated genetic manipulations in mice have now allowed dissecting these mechanisms with greater accuracy. Here we discuss some recent papers that provided novel insights into how these different mapping rules and constraints interact to shape the barrel map.
Topics: Afferent Pathways; Animals; Brain Mapping; Gene Expression; Somatosensory Cortex; Touch Perception; Vibrissae
PubMed: 29753205
DOI: 10.1016/j.conb.2018.04.028 -
Proceedings of the National Academy of... Mar 2021For neuronal circuits in the brain to mature, necessary synapses must be maintained and redundant synapses eliminated through experience-dependent mechanisms. However,...
For neuronal circuits in the brain to mature, necessary synapses must be maintained and redundant synapses eliminated through experience-dependent mechanisms. However, the functional differentiation of these synapse types during the refinement process remains elusive. Here, we addressed this issue by distinct labeling and direct recordings of presynaptic terminals fated for survival and for elimination in the somatosensory thalamus. At surviving terminals, the number of total releasable vesicles was first enlarged, and then calcium channels and fast-releasing synaptic vesicles were tightly coupled in an experience-dependent manner. By contrast, transmitter release mechanisms did not mature at terminals fated for elimination, irrespective of sensory experience. Nonetheless, terminals fated for survival and for elimination both exhibited developmental shortening of action potential waveforms that was experience independent. Thus, we dissected experience-dependent and -independent developmental maturation processes of surviving and eliminated presynaptic terminals during neuronal circuit refinement.
Topics: Action Potentials; Afferent Pathways; Animals; Calcium Channels; Mice; Nerve Net; Neurotransmitter Agents; Presynaptic Terminals; Synaptic Vesicles; Trigeminal Nuclei; Ventral Thalamic Nuclei; Vibrissae
PubMed: 33688051
DOI: 10.1073/pnas.2022423118 -
Nature Neuroscience Jan 2017Anatomical, stimulation and lesion data implicate vibrissa motor cortex in whisker motor control. Work on motor cortex has focused on movement generation, but...
Anatomical, stimulation and lesion data implicate vibrissa motor cortex in whisker motor control. Work on motor cortex has focused on movement generation, but correlations between vibrissa motor cortex activity and whisking are weak. The exact role of vibrissa motor cortex remains unknown. We recorded vibrissa motor cortex neurons during various forms of vibrissal touch, which were invariably associated with whisker protraction and movement. Free whisking, object palpation and social touch all resulted in decreased cortical activity. To understand this activity decrease, we performed juxtacellular recordings, nanostimulation and in vivo whole-cell recordings. Social touch resulted in decreased spiking activity, decreased cell excitability and membrane hyperpolarization. Activation of vibrissa motor cortex by intracortical microstimulation elicited whisker retraction, as if to abort vibrissal touch. Various vibrissa motor cortex inactivation protocols resulted in contralateral protraction and increased whisker movements. These data collectively point to movement suppression as a prime function of vibrissa motor cortex activity.
Topics: Action Potentials; Animals; Behavior, Animal; Mice, Inbred C57BL; Motor Cortex; Motor Neurons; Movement; Patch-Clamp Techniques; Rats, Wistar; Somatosensory Cortex; Vibrissae
PubMed: 27798633
DOI: 10.1038/nn.4437